Asymmetric and Spiraled Genitalia Coevolve with Unique Lateralized Mating Behavior

Dara N Orbach,Marc A Webber,Sarah L Mesnick,William Keener,Patricia L R Brennan,Brandon P Hedrick

doi:10.1038/s41598-020-60287-w

Abstract

Asymmetric genitalia and lateralized mating behaviors occur in several taxa, yet whether asymmetric morphology in one sex correlates or coevolves with lateralized mating behavior in the other sex remains largely unexplored. While lateralized mating behaviors are taxonomically widespread, among mammals they are only known in the harbor porpoise (Phocoena phocoena). Males attempt copulation by approaching a female exclusively on her left side. To understand if this unusual lateralized behavior may have coevolved with genital morphology, we quantified the shape of female and male harbor porpoise reproductive tracts using 2D geometric morphometrics and 3D models of the vaginal lumen and inflated distal penis. We found that the vaginas varied individually in shape and that the vaginas demonstrated both significant directional and fluctuating asymmetry. This asymmetry resulted from complex 3D spirals and vaginal folds with deep recesses, which may curtail the depth or direction of penile penetration and/or semen movement. The asymmetric shapes of the vaginal lumen and penis tip were both left-canted with similar angular bends that mirrored one another and correspond with the left lateral mating approach. We suggest that the reproductive anatomy of both sexes and their lateral mating behavior coevolved.

Highlights

Left- or right-bias in morphology and behavior in otherwise bilaterally symmetrical animals manifests in diverse biological phenomena such as mating, foraging, predation, predator defense, and communication[1,2]
We explored the coevolution of genital morphology and mating behavior asymmetry between male and female harbor porpoises, the only mammal known to demonstrate exclusive lateralized mating behavior
We provide evidence that genital asymmetry has coevolved with lateralized mating behavior in harbor porpoises, the first example amongst mammals

Summary

Introduction

Left- or right-bias in morphology and behavior in otherwise bilaterally symmetrical animals manifests in diverse biological phenomena such as mating, foraging, predation, predator defense, and communication[1,2]. Copulatory attempts consisted of rapid (1–4 seconds), high-energy, precision-timed approaches, during which the males often breached out of the water with their penis fully extended and attempted to drive their penis into the female’s vaginal opening[7] The complexity of their genital morphology and their lateralized mating behavior make the harbor porpoise an exemplary taxon to explore the potential relationship between reproductive morphology and mating behavior. We examined the pattern of asymmetry in vaginal folds in both 2D and 3D by generating models of the vaginal lumen, in addition to assessing gross morphology This is the first study to address the question of whether lateralized mating behaviors affect genital morphology in mammals, and allows for a better understanding of the drivers of sexual patterns in both cetaceans and the wide variety of animals that have asymmetric genitalia with potentially previously unrecognized lateralized mating behaviors

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Conclusion